IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-27413-2.html
   My bibliography  Save this article

Computational mechanisms of distributed value representations and mixed learning strategies

Author

Listed:
  • Shiva Farashahi

    (Dartmouth College
    Center for Computational Neuroscience, Flatiron Institute, Simons Foundation)

  • Alireza Soltani

    (Dartmouth College)

Abstract

Learning appropriate representations of the reward environment is challenging in the real world where there are many options, each with multiple attributes or features. Despite existence of alternative solutions for this challenge, neural mechanisms underlying emergence and adoption of value representations and learning strategies remain unknown. To address this, we measure learning and choice during a multi-dimensional probabilistic learning task in humans and trained recurrent neural networks (RNNs) to capture our experimental observations. We find that human participants estimate stimulus-outcome associations by learning and combining estimates of reward probabilities associated with the informative feature followed by those of informative conjunctions. Through analyzing representations, connectivity, and lesioning of the RNNs, we demonstrate this mixed learning strategy relies on a distributed neural code and opponency between excitatory and inhibitory neurons through value-dependent disinhibition. Together, our results suggest computational and neural mechanisms underlying emergence of complex learning strategies in naturalistic settings.

Suggested Citation

  • Shiva Farashahi & Alireza Soltani, 2021. "Computational mechanisms of distributed value representations and mixed learning strategies," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27413-2
    DOI: 10.1038/s41467-021-27413-2
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-27413-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-021-27413-2?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Valerio Mante & David Sussillo & Krishna V. Shenoy & William T. Newsome, 2013. "Context-dependent computation by recurrent dynamics in prefrontal cortex," Nature, Nature, vol. 503(7474), pages 78-84, November.
    2. R. Quian Quiroga & L. Reddy & G. Kreiman & C. Koch & I. Fried, 2005. "Invariant visual representation by single neurons in the human brain," Nature, Nature, vol. 435(7045), pages 1102-1107, June.
    3. Shiva Farashahi & Katherine Rowe & Zohra Aslami & Daeyeol Lee & Alireza Soltani, 2017. "Feature-based learning improves adaptability without compromising precision," Nature Communications, Nature, vol. 8(1), pages 1-16, December.
    4. Alireza Soltani & Peyman Khorsand & Clara Guo & Shiva Farashahi & Janet Liu, 2016. "Neural substrates of cognitive biases during probabilistic inference," Nature Communications, Nature, vol. 7(1), pages 1-14, September.
    5. Johannes J. Letzkus & Steffen B. E. Wolff & Elisabeth M. M. Meyer & Philip Tovote & Julien Courtin & Cyril Herry & Andreas Lüthi, 2011. "A disinhibitory microcircuit for associative fear learning in the auditory cortex," Nature, Nature, vol. 480(7377), pages 331-335, December.
    6. Mariann Oemisch & Stephanie Westendorff & Marzyeh Azimi & Seyed Alireza Hassani & Salva Ardid & Paul Tiesinga & Thilo Womelsdorf, 2019. "Feature-specific prediction errors and surprise across macaque fronto-striatal circuits," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    7. Amir Dezfouli & Kristi Griffiths & Fabio Ramos & Peter Dayan & Bernard W Balleine, 2019. "Models that learn how humans learn: The case of decision-making and its disorders," PLOS Computational Biology, Public Library of Science, vol. 15(6), pages 1-33, June.
    8. Mehran Spitmaan & Oihane Horno & Emily Chu & Alireza Soltani, 2019. "Combinations of low-level and high-level neural processes account for distinct patterns of context-dependent choice," PLOS Computational Biology, Public Library of Science, vol. 15(10), pages 1-31, October.
    9. Peyman Khorsand & Alireza Soltani, 2017. "Optimal structure of metaplasticity for adaptive learning," PLOS Computational Biology, Public Library of Science, vol. 13(6), pages 1-22, June.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Amir Dezfouli & Bernard W Balleine, 2019. "Learning the structure of the world: The adaptive nature of state-space and action representations in multi-stage decision-making," PLOS Computational Biology, Public Library of Science, vol. 15(9), pages 1-22, September.
    2. Micha Heilbron & Florent Meyniel, 2019. "Confidence resets reveal hierarchical adaptive learning in humans," PLOS Computational Biology, Public Library of Science, vol. 15(4), pages 1-24, April.
    3. Matteo Farinella & Daniel T Ruedt & Padraig Gleeson & Frederic Lanore & R Angus Silver, 2014. "Glutamate-Bound NMDARs Arising from In Vivo-like Network Activity Extend Spatio-temporal Integration in a L5 Cortical Pyramidal Cell Model," PLOS Computational Biology, Public Library of Science, vol. 10(4), pages 1-21, April.
    4. Umut Güçlü & Marcel A J van Gerven, 2014. "Unsupervised Feature Learning Improves Prediction of Human Brain Activity in Response to Natural Images," PLOS Computational Biology, Public Library of Science, vol. 10(8), pages 1-12, August.
    5. Payam Piray & Nathaniel D Daw, 2020. "A simple model for learning in volatile environments," PLOS Computational Biology, Public Library of Science, vol. 16(7), pages 1-26, July.
    6. Georgia Koppe & Hazem Toutounji & Peter Kirsch & Stefanie Lis & Daniel Durstewitz, 2019. "Identifying nonlinear dynamical systems via generative recurrent neural networks with applications to fMRI," PLOS Computational Biology, Public Library of Science, vol. 15(8), pages 1-35, August.
    7. Jan Weber & Anne-Kristin Solbakk & Alejandro O. Blenkmann & Anais Llorens & Ingrid Funderud & Sabine Leske & Pål Gunnar Larsson & Jugoslav Ivanovic & Robert T. Knight & Tor Endestad & Randolph F. Helf, 2024. "Ramping dynamics and theta oscillations reflect dissociable signatures during rule-guided human behavior," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    8. Pierre O. Boucher & Tian Wang & Laura Carceroni & Gary Kane & Krishna V. Shenoy & Chandramouli Chandrasekaran, 2023. "Initial conditions combine with sensory evidence to induce decision-related dynamics in premotor cortex," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    9. Rishi Rajalingham & Aída Piccato & Mehrdad Jazayeri, 2022. "Recurrent neural networks with explicit representation of dynamic latent variables can mimic behavioral patterns in a physical inference task," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    10. Athina Tzovara & Christoph W Korn & Dominik R Bach, 2018. "Human Pavlovian fear conditioning conforms to probabilistic learning," PLOS Computational Biology, Public Library of Science, vol. 14(8), pages 1-21, August.
    11. Rodrigo Quian Quiroga & Marta Boscaglia & Jacques Jonas & Hernan G. Rey & Xiaoqian Yan & Louis Maillard & Sophie Colnat-Coulbois & Laurent Koessler & Bruno Rossion, 2023. "Single neuron responses underlying face recognition in the human midfusiform face-selective cortex," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    12. Wan-Yu Shih & Hsiang-Yu Yu & Cheng-Chia Lee & Chien-Chen Chou & Chien Chen & Paul W. Glimcher & Shih-Wei Wu, 2023. "Electrophysiological population dynamics reveal context dependencies during decision making in human frontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    13. Wenyi Zhang & Yang Xie & Tianming Yang, 2022. "Reward salience but not spatial attention dominates the value representation in the orbitofrontal cortex," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    14. Nir Even-Chen & Blue Sheffer & Saurabh Vyas & Stephen I Ryu & Krishna V Shenoy, 2019. "Structure and variability of delay activity in premotor cortex," PLOS Computational Biology, Public Library of Science, vol. 15(2), pages 1-17, February.
    15. Amir Bagherpour, 2021. "How computer simulations enhance geopolitical decision‐making: A commentary on Lustick and Tetlock 2021," Futures & Foresight Science, John Wiley & Sons, vol. 3(2), June.
    16. Javier G. Orlandi & Mohammad Abdolrahmani & Ryo Aoki & Dmitry R. Lyamzin & Andrea Benucci, 2023. "Distributed context-dependent choice information in mouse posterior cortex," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    17. Martinez-Saito, Mario, 2022. "Discrete scaling and criticality in a chain of adaptive excitable integrators," Chaos, Solitons & Fractals, Elsevier, vol. 163(C).
    18. Luca D. Kolibius & Frederic Roux & George Parish & Marije Wal & Mircea Plas & Ramesh Chelvarajah & Vijay Sawlani & David T. Rollings & Johannes D. Lang & Stephanie Gollwitzer & Katrin Walther & Rüdige, 2023. "Hippocampal neurons code individual episodic memories in humans," Nature Human Behaviour, Nature, vol. 7(11), pages 1968-1979, November.
    19. Jakub Kopal & Kuldeep Kumar & Kimia Shafighi & Karin Saltoun & Claudia Modenato & Clara A. Moreau & Guillaume Huguet & Martineau Jean-Louis & Charles-Olivier Martin & Zohra Saci & Nadine Younis & Elis, 2024. "Using rare genetic mutations to revisit structural brain asymmetry," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    20. Joao Barbosa & Rémi Proville & Chris C. Rodgers & Michael R. DeWeese & Srdjan Ostojic & Yves Boubenec, 2023. "Early selection of task-relevant features through population gating," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27413-2. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.